Catabolic pathway of arginine in Anabaena involves a novel bifunctional enzyme that produces proline from arginine

Abstract

Summary Arginine participates widely in metabolic processes. The heterocyst‐forming cyanobacterium Anabaena catabolizes arginine to produce proline and glutamate, with concomitant release of ammonium, as major products. Analysis of mutant Anabaena strains showed that this catabolic pathway is the product of two genes, agrE (alr4995) and putA (alr0540). The predicted PutA protein is a conventional, bifunctional proline oxidase that produces glutamate from proline. In contrast, AgrE is a hitherto unrecognized enzyme that contains both an N‐terminal α/β propeller domain and a unique C‐terminal domain of previously unidentified function. In vitro analysis of the proteins expressed in Escherichia coli or Anabaena showed arginine dihydrolase activity of the N‐terminal domain and ornithine cyclodeaminase activity of the C‐terminal domain, overall producing proline from arginine. In the diazotrophic filaments of Anabaena, β‐aspartyl‐arginine dipeptide is transferred from the heterocysts to the vegetative cells, where it is cleaved producing aspartate and arginine. Both agrE and putA were found to be expressed at higher levels in vegetative cells than in heterocysts, implying that arginine is catabolized by the AgrE‐PutA pathway mainly in the vegetative cells. Expression in Anabaena of a homolog of the C‐terminal domain of AgrE obtained from Methanococcus maripaludis enabled us to identify an archaeal ornithine cyclodeaminase.

Arginine and nitrogen mobilization in cyanobacteria

“…The finding by Burnat, Picossi et al () provides a more complete understanding of arginine metabolism in Anabaena . Moreover, this study identified the C‐terminal domain of AgrE/ArgZ as an ornithine cyclodeaminase that catalyze the conversion of ornithine to proline.…”

“…Burnat et al () identified the arginine catabolic pathway in a diazotrophic cyanobacterium Anabaena sp. PCC 7120.…”

“…These results indicate that AgrE is involved in conversion of arginine to proline and that PutA catalyzes the conversion of proline to glutamate in Anabaena . The C‐terminal domain of AgrE/ArgZ protein is homologous to a Methanococcus protein MMP1218 (referred to as Mls2 by Burnat, Picossi et al , ), and indeed heterologous expression of MMP1218 resulted in synthesis of proline from ornithine in Anabaena . Furthermore, the authors performed biochemical assays using purified AgrE protein from Anabaena .…”

“…A recent study identified an arginine dihydrolase encoded by gene argZ (designated as agrE by Burnat, Picossi et al, 2019), which catalyzes the conversion of arginine into ornithine and ammonia ( Fig. 1) (Zhang et al, 2018).…”

“…Moreover, the function of the C-terminal domain of ArgZ/ AgrE protein was still unknown. Burnat et al (2019) identified the arginine catabolic pathway in a diazotrophic cyanobacterium Anabaena sp. PCC 7120.…”